Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2020 Dec 18;7(1):veaa095.
doi: 10.1093/ve/veaa095. eCollection 2021 Jan.

Divergent RNA viruses in Macrophomina phaseolina exhibit potential as virocontrol agents

Jing Wang  1   2 , Yunxia Ni  1 , Xintao Liu  1 , Hui Zhao  1 , Yannong Xiao  3 , Xueqiong Xiao  3 , Shujun Li  2 , Hongyan Liu  1
Affiliations

Divergent RNA viruses in Macrophomina phaseolina exhibit potential as virocontrol agents

Jing Wang et al. Virus Evol. .

Abstract

Macrophomina phaseolina is an important necrotrophic phytopathogenic fungus and cause extensive damage in many oilseed crops. Twelve M.phaseolina isolates with diverse biological phenotypes were selected for a high-throughput sequencing-based metatranscriptomic and bioinformatics analysis to identify viruses infecting M.phaseolina. The analysis identified 40 partial or nearly complete viral genome segments, 31 of which were novel viruses. Among these viral sequences, 43% of the viral genomes were double-stranded RNA (dsRNA), 47% were positive single-stranded RNA (ssRNA+), and the remaining 10% were negative sense-stranded RNA (ssRNA-). The 40 viruses showed affinity to 13 distinct viral lineages, including Bunyavirales (four viruses), Totiviridae (three viruses), Chrysoviridae (five viruses), Partitiviridae (four viruses), Hypoviridae (one virus), Endornaviridae (two viruses), Tombusviridae (three viruses), Narnaviridae (one virus), Potyviridae (one virus), Bromoviridae (one virus), Virgaviridae (six viruses), 'Fusagraviridae' (five viruses), and Ourmiavirus (four viruses). Two viruses are closely related to two families, Potyviridae and Bromoviridae, which previously contained no mycovirus species. Moreover, nine novel viruses associated with M.phaseolina were identified in the family Totiviridae, Endornaviridae, and Partitiviridae. Coinfection with multiple viruses is prevalent in M.phaseolina, with each isolate harboring different numbers of viruses, ranging from three to eighteen. Furthermore, the effects of the viruses on the fungal host were analyzed according to the biological characteristics of each isolate. The results suggested that M.phaseolina hypovirus 2, M.phaseolina fusagravirus virus 1-5 (MpFV1-5), M.phaseolina endornavirus 1-2 (MpEV1-2), M.phaseolina ourmia-like virus 1-3 (MpOLV1-3), M.phaseolina mitovirus 4 (MpMV4), and M.phaseolina mycobunyavirus 1-4 (MpMBV1-4) were only detected in hypovirulent isolates. Those viruses associated with hypovirulence might be used as biological control agents as an environmentally friendly alternative to chemical fungicides. These findings considerably expand our understanding of mycoviruses in M.phaseolina and unvailed the presence of a huge difference among viruses in isolates from different hosts in distant geographical regions. Together, the present study provides new knowledge about viral evolution and fungus-virus coevolution.

Keywords: Macrophomina phaseolina; coinfection; diversity; hypovirulence; metatranscriptomic; mycovirus.

PubMed Disclaimer

Figures

Figure 1.
Figure 1.
The reverse transcription (RT)-PCR detection of mycovirus contigs in Macrophomina phaseolina strains with primer pairs and predicted sizes of amplicons are listed in Supplementary Table S1. Lane M, DL2000 DNA Marker (Takara Bio Inc., Japan); Lane 1 to 12, 12 M.phaseolina strains tested in this study (see Supplementary Table S1 for details); abbreviates of viruses are on the far right side of the lane.
Figure 2.
Figure 2.
Genome organizations and phylogenetic analysis of the putative negative-stranded RNA virus genomes detected from Macrophomina phaseolina. (A) Comparison of the organizations of putative negative-stranded RNA viruses M.phaseolina mycobunyavirus 1 (MpMBV1) and M.phaseolina mycobunyavirus 3 (MpMBV3) to Botrytis cinerea negative-stranded RNA virus 1 (BcNSRV1), and M.phaseolina negative-stranded RNA virus 1 (MpNSRV1), respectively. Open reading frame (ORF) is shown as colored box. The horizontal line represent conserved domain. The numbers in the dotted line represent identity between viruses. (B) Neighbor joining tree depicting the relationships of the predicted RdRp amino acid sequences were aligned with CLUSTALX, and trees were inferred using MEGA-X. The viruses marked with red dot are found in M.phaseolina.
Figure 3.
Figure 3.
Genome organizations and phylogenetic analysis of the putative viruses in family Endornaviridae and Hypoviridae. (A) Comparison of the organizations of putative viruses Macrophomina phaseolina endornavirus 1 (MpEV1) and M.phaseolina endornavirus 2 (MpEV2) to Hordeum vulgare endornavirus (HvEV1), and M.phaseolina Hypovirus 2 (MpHV2) to M.phaseolina Hypovirus 1 (MpHV1). (B) Predicted RdRp amino acid sequences of endornaviruses and hypovirus were aligned and phylogenetic tree were constructed as described in Fig. 1. The viruses marked with red dot or red diamonds are found in M.phaseolina.
Figure 4.
Figure 4.
Genome organizations and phylogenetic analysis of the putative viruses in family Chrysoviridae detected from Macrophomina phaseolina. (A) Comparison of the organizations of putative viruses M.phaseolina chrysovirus 2 (MpChrV2), M.phaseolina chrysovirus 3 (MpChrV3), and M.phaseolina chrysovirus 4 (MpChrV4) to Aspergillus fumigatus chrysoviurs, Aspergillus thermomutatus chrysoviurs 1, and Colletotrichum fructicola chrysoviurs 1, respectively. (B) Predicted RdRp amino acid sequences of chrysovirus were aligned and phylogenetic tree were constructed as described in Fig. 1. The viruses marked with red dot were found in M.phaseolina.
Figure 5.
Figure 5.
Genome organizations and phylogenetic analysis of the putative viruses in family ‘Fusagraviridae’, Totiviridae, and Partitiviridae detected from Macrophomina phaseolina. (A) Comparison of the organizations of putative viruses M.phaseolina fusagravirus 2 (MpFV2), M.phaseolina fusagravirus 3 (MpFV3), M.phaseolina fusagravirus 4 (MpFV4), and M.phaseolina fusagravirus 5 (MpFV5) to M.phaseolina double-stranded RNA virus 2 (MpRV2). Comparison of the organizations of putative viruses M.phaseolina victorivirus 2 (MpV2) to Sphaeropsis sapinea RNA virus 2 (SsRV2). Comparison of the organizations of putative viruses M.phaseolina partitivirus 1 (MpPV1) and M.phaseolina partitivirus 2 (MpPV2) to Ustilaginoidea virens partitivirus 3 (UvPV3) and Fusarium solani virus 1 (FsV1), respectively. (B) Predicted RdRp amino acid sequences of MpFV2, MpFV3, MpFV4, MpFV5, MpV2, MpPV1, and MpPV2 were aligned and phylogenetic tree were constructed as described in Fig. 1. The viruses marked with red diamonds, red dots, and red squares were found in M.phaseolina.
Figure 6.
Figure 6.
Genome organizations and phylogenetic analysis of the putative viruses in family Potyviridae, Tombusviridae, and Bromoviridae detected from Macrophomina phaseolina. (A) Comparison of the organizations of putative viruses M.phaseolina umbra-like virus 1 (MpULV1) and M.phaseolina umbra-like virus 3 (MpULV3) to Sclerotinia sclerotiorum umbra-like virus 1 (SsULV1). Comparison of the organizations of putative viruses M.phaseolina poty-like virus (MpPLV) to Watermelon mosaic virus (WMV). Comparison of the organizations of putative viruses M.phaseolina ilar-like virus (MpILV) to Tomato necrotic streak virus (TNSV). (B) Predicted RdRp amino acid sequences of MpULV1, MpULV3, MpPLV, and MpILV were aligned and phylogenetic tree were constructed as described in Fig. 1. The viruses marked with red dots, red squares, and red diamonds were found in M.phaseolina.
Figure 7.
Figure 7.
Genome organizations and phylogenetic analysis of the putative viruses in genus Ourmiavirus and mitovirus detected from Macrophomina phaseolina. (A) Comparison of the organizations of putative viruses M.phaseolina ourmia-like virus 1 (MpOLV1), M.phaseolina ourmia-like virus 2 (MpOLV2), M.phaseolina ourmia-like virus 2-A (MpOLV2-A), and M.phaseolina ourmia-like virus 3 (MpOLV3) to Erysiphe necator associated ourmia-like virus 8 (EnOLV8), Acremonium sclerotigenum ourmia-like virus 1 (AsOLV1), and Neofusicoccum parvum ourmia-like virus 1 (NpOLV1), respectively. Comparison of the organizations of putative viruses M.phaseolina mitovirus 1 (MpMV1) to and Rhizoctonia solani mitovirus 10 (RsMV10). (B) Predicted RdRp amino acid sequences of MpOLV1, MpOLV2, MpOLV2-A, MpOLV3, and MpPLV, and MpILV were aligned and phylogenetic tree were constructed as described in Fig. 1. The viruses marked with red dots, red squares, and red diamonds were found in M.phaseolina.
Figure 8.
Figure 8.
Genome organizations and phylogenetic analysis of the putative viruses in family Virgaviridae detected from Macrophomina phaseolina. (A) Comparison of the organizations of putative viruses M.phaseolina tobamo-like virus 2 (MpTLV2) to M.phaseolina tobamo-like virus (MpTLV). (B) Predicted RdRp amino acid sequences of MpTLV2 and other Tobamo-like viruses were aligned and phylogenetic tree were constructed as described in Fig. 1. The viruses marked with red dots were found in M.phaseolina.
Figure 9.
Figure 9.
The comparison of different biological characteristic and quantity of mycoviruses among 12 isolates of Macrophomina phaseolina. (A) Compare the colony morphology, hyphal tips, and virulence of 12 isolates. All fungal strains were grown on PDA for 4 days at 30°C and photographed. (B) Growth rate of 12 isolates were measured on PDA for 48 h at 30°C. (C) Biomass of 12 isolates was measured in PDB for 8 days at 30°C. (D) The data of pathogenicity was calculated base on RAUDPC. (E) The number of ssRNA−, ssRNA+, and dsRNA viruses contained by 12 isolates respectively. Means followed by the different letters on the top of each column are significantly different at the P < 0.05 level of confidence according to Duncan’s multiple range test.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Adams M. J., Antoniw J. F., Kreuze J. (2009) ‘ Virgaviridae: A New Family of Rod-Shaped Plant Viruses’, Archives of Virology, 154: 1967–72. - PubMed
    1. Adams Z. (2012) ‘Family Potyviridae’, in King A.M.Q., Adams M.J., Carstens E.B., Lefkowitz E.J. (eds.) Virus Taxonomy: Classification and Nomenclature of Viruses, Ninth Report of the International Committee on Taxonomy of Viruses, pp.1069–89. Waltham, MA, USA.
    1. Aiewsakun P., Katzourakis A. (2015) ‘ Endogenous Viruses: Connecting Recent and Ancient Viral Evolution’, Virology, 479–480: 26–37. - PubMed
    1. Amarasinghe G. K. et al. (2017) ‘ Taxonomy of the Order Mononegavirales: Update 2017’, Archives of Virology, 162: 2493–504. - PMC - PubMed
    1. Ammon V., Wyllie T. D., Brown M. F. (1974) ‘ An Ultrastructural Investigation of Pathological Alterations Induced by Macrophomina Phaseolina (Tassi) Goid in Seedlings of Soybean, Glycine max (L.) Merrill’, Physiological Plant Pathology, 4: 1–4.
开云球赛中国有限公司 | 万搏官方网站 | c7官网登录入口 | 九州平台-九州(中国) | 万搏官方网站 | 千亿球友会·(中国)官方网站 | 米兰体育网址 | 开云手机官方网站 | 江南手机网页版登录入口 |